Anthropogenic landscapes increase Campylobacter jejuni infections in urbanizing banded mongoose ( Mungos mungo): A one health approach

Abstract

Background

Campylobacter is a common, but neglected foodborne-zoonotic pathogen, identified as a growing cause of foodborne disease worldwide. Wildlife and domestic animals are considered important reservoirs, but little is known about pathogen infection dynamics in free-ranging mammalian wildlife particularly in sub-Saharan Africa. In countries like Botswana, there is significant overlap between humans and wildlife, with the human population having one of the highest HIV infection rates in the world, increasing vulnerability to infection.

Methodology/Principal findings

We investigated Campylobacter occurrence in archived human fecal samples (children and adults, n = 122, 2011), feces from free-ranging banded mongooses ( Mungos mungo, n = 201), surface water (n = 70), and river sediment samples (n = 81) collected in 2017 from the Chobe District, northern Botswana. Campylobacter spp. was widespread in humans (23.0%, 95% CI 13.9–35.4%), with infections dominantly associated with C. jejuni (82.1%, n = 28, 95% CI 55.1–94.5%). A small number of patients presented with asymptomatic infections (n = 6). While C ampylobacter spp. was rare or absent in environmental samples, over half of sampled mongooses tested positive (56%, 95% CI 45.6–65.4%). Across the urban-wilderness continuum, we found significant differences in Campylobacter spp. detection associated with the type of den used by study mongooses. Mongooses utilizing man-made structures as den sites had significantly higher levels of C. jejuni infection (p = 0.019) than mongooses using natural dens. Conversely, mongooses using natural dens had overall higher levels of detection of Campylobacter at the genus level (p = 0.001).

Conclusions

These results suggest that landscape features may have important influences on Campylobacter species exposure and transmission dynamics in wildlife. In particular, data suggest that human-modified landscapes may increase C. jejuni infection, a primarily human pathogen, in banded mongooses. Pathogen circulation and transmission in urbanizing wildlife reservoirs may increase human vulnerability to infection, findings that may have critical implications for both public and animal health in regions where people live in close proximity to wildlife.

Author summary

Campylobacter infections are increasing worldwide but we still know little about the true burden of disease in the developing world, and even less about the role of wildlife and environmental reservoirs in human exposure and infection. Here we take a one-health approach evaluating Campylobacter infections in humans, banded mongooses ( Mungos mungo), and the environment. We found evidence of widespread infection with Campylobacter spp. infecting nearly a quarter of sampled adults and children (23.0%, n = 122, 2011), dominantly with C. jejuni. Banded mongooses live in close association with humans in the area and over half of the animals sampled were found positive for Campylobacter spp. (56%, n = 201, 2017). Infection with C. jejuni was greater among mongooses utilizing human-made structures as den sites than those using natural dens. These data suggest that wildlife utilization of anthropogenic landscapes may increase C. jejuni exposure and infection. In turn, pathogen circulation and transmission in urbanizing wildlife reservoirs may increase human vulnerability to infection, particularly impoverished populations, where greater environmental exposures are expected.